Phylogenetic considerations of clonality, coloniality, and mode of germline development in animals

Blackstone, Neil W.; Jasker, Bryan D.

doi:10.1002/jez.b.16

Cited by 74 publications

(69 citation statements)

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“…By contrast, studies in animals that can propagate asexually suggest that germline precursors can also originate in adults, from either pluripotent stem cells that can give rise to somatic or germline fate, or de-and/or transdifferentiation of cells and tissues (Blackstone and Jasker, 2003;Extavour et al, 2005;Nieuwkoop and Sutasurya, 1979;Nieuwkoop and Sutasurya, 1981).…”

Section: Introductionmentioning

confidence: 99%

Early lineage specification of long-lived germline precursors in the colonial ascidianBotryllus schlosseri

et al. 2009

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DEVELOPMENT 3486bodies undergo apoptosis and are removed via phagocytic cells in the blood, the primary bud migrates into the newly vacated region of the colony, opening its siphons and becoming a zooid, the secondary bud becomes the primary bud, and a new secondary bud begins to develop. Thus, the life history of Botryllus consists of a constant succession of individual zooids, each with a three-week lifespan (Lauzon et al., 2002).Asexual development (blastogenesis) takes 14 days under laboratory conditions, and can be divided into seven distinct visual stages ( Fig. 1; stages A-1 through D) (Lauzon et al., 2002). A new generation starts as a secondary bud, first visible as a thickening of the peribranchial epithelium of a primary bud ( Fig. 1; stage A1), which evaginates and forms a closed vesicle ( Fig. 1; stage A-2 through B-2). Next, a series of epithelial invaginations and protrusions ( Fig. 1; stage C-1) differentiate into somatic tissues and organs ( Fig. 1; stage C-2). After seven days ( Fig. 1; stage D), the secondary bud transitions to a primary bud and continues to develop. At day 14, the siphons open and the primary bud becomes a filterfeeding adult zooid. Each zooid can generate multiple buds each week, so the colony will eventually expand asexually. While interconnected, the zooids and buds develop independently, and individuals can be separated from the colony without disturbing their growth (i.e. subcloning), thus multiple experiments can be done on a single genotype.Following metamorphosis, colonies undergo at least 8-12 developmental cycles prior to the first appearance of gametes (sexual maturity). In addition, populations show seasonal fertility, and in the lab cycle in and out of reproductive (fertile) and nonreproductive (infertile) states. However when the colony is fertile development of the gametes is synchronized with somatic development (Mukai, 1977;Mukai and Watanabe, 1976;Sabbadin and Zaniolo, 1979). The first appearance of gonads occurs in the secondary bud (stage B), when mobile progenitors in the blood migrate to a region between the inner epithelium and the epidermis and begin to proliferate. Concurrently, oocytes at various stages of development also appear (Fig. 1). Over the next 10 days, the medial region of the blastema will differentiate into the lobular testis, while the lateral region will become the ovary (Sabbadin and Zaniolo, 1979). For the latter, one or several oocytes will become fixed on the epithelia of the peribranchial chamber, and an oviduct will form from the outer follicular layer. Upon transition to the adult zooid, mature eggs will immediately ovulate into the peribranchial chamber, be fertilized by exogenous sperm, and develop in situ. Several hours to days later the testes will complete development, and sperm will be released into the peribranchial chamber and flushed into the water column, fertilizing neighboring colonies (Johnson and Yund, 2004). The time lag between ovulation and sperm release (protogyny) prevents self-fertilization.Given this plastici...

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Section: Introductionmentioning

confidence: 99%

Early lineage specification of long-lived germline precursors in the colonial ascidianBotryllus schlosseri

et al. 2009

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“…This is, however, unsupported for plants, fungi, most multicellular protists (e.g., seaweeds), and at least 19 animal phyla (Buss 1983). Distinct germ lines are notably absent in all organisms capable of somatic embryogenesis (ramet formation via mitotic cell lineages such as fragments or spores), which usually coincides with colonial or modular growth (Buss 1983;Blackstone and Jasker 2003). Such capacity requires that at least some propagative cells (e.g., meristems) remain totipotent throughout an individual's lifespan, unlike such cells in so-called preformistic taxa (mostly arthropods and chordates), which undergo terminal differentiation in early ontogeny (Buss 1987).…”

Section: Introductionmentioning

confidence: 99%

The Potential for Evolutionary Responses to Cell‐Lineage Selection on Growth Form and Its Plasticity in a Red Seaweed

Monro

Poore

2009

The American Naturalist

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JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.. abstract: Despite much theoretical discussion on the evolutionary significance of intraclonal genetic variation, particularly for modular organisms whose lack of germ-soma segregation allows for variants arising in clonal growth to contribute to evolutionary change, the potential of this variation to fuel adaptation remains surprisingly untested. Given intraclonal variation, mitotic cell lineages, rather than sexual offspring, may frequently act as units of selection. Here, we applied artificial selection to such lineages in the branching red seaweed Asparagopsis armata, targeting aspects of clonal growth form and growth-form plasticity that enhance light acquisition on patchy subtidal reefs and predicting that a genetic basis to intraclonal variation may promote significant responses that cannot accompany phenotypic variation alone. Cell-lineage selection increased variation in branch proliferation among A. armata genets and successfully altered its plasticity to light. Correlated responses in the plasticity of branch elongation, moreover, showed that cell-lineage selection may be transmitted among the plasticities of growth-form traits in A. armata via pleiotropy. By demonstrating significant responses to celllineage selection on growth-form plasticity in this seaweed, our study lends support to the notion that intraclonal genetic variation may potentially help clonal organisms to evolve adaptively in the absence of sex and thereby prove surprisingly resilient to environmental change.

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“…The term "somatic embryogenesis" (Buss, 1987;Blackstone & Jasker, 2003) suggests that stem cells, which ensure the asexual reproduction, are recognized as somatic ones; pluripotent stem cells in animals with asexual reproduction are often referred as somatic (Blackstone & Jasker, 2003;Extavour & Akam, 2003;Rinkevich, 2009;Sköld et al, 2009;Funayama et al, 2010). However, pluriponent gametogenic stem cells of asexually reproducing invertebrates, like primary germ cells, do not belong to any germ layer, differentiated tissue, and population of specialized somatic cells or their somatic stem cells (Isaeva, 2010(Isaeva, , 2011.…”

Section: Resultsmentioning

confidence: 99%

“…Examples of such pluripotent gametogenic stem cells include sponge archaeocytes, cnidarian interstitial cells, planarian neoblasts, ascidian hemoblasts and stem cells of colonial rhizocephalans (reviews: Isaeva et al, 2008Isaeva et al, , 2009Rinkevich et al, 2009;Sköld et al, 2009;Srouji & Extavour, 2011). In addition to the germline segregation by preformation, or mosaic developmental mode and epigenesis, or regulative mode Extavour & Akam, 2003;Gustafson & Wessel, 2010), somatic embryogenesis was also recognized (Buss, 1987;Blackstone & Jasker, 2003;Gustafson & Wessel, 2010;Rinckevich et al, 2009;Rosner et al, 2009). Earlier, somatic embryogenesis as natural cloning in animals was termed blastogenesis (Berrill, 1961;Ivanova-Kazas, 1996).…”

Section: Introductionmentioning

confidence: 99%

“…In the life cycle of colonial animals, one generation of oozooid (an individual that has developed from an egg) alternates with numerous generations of blastozooids, with alternating morphogenetic processes: embryogenesis and blastogenesis (Ivanova-Kazas, 1996). Many animals, including placozoans, sponges, cnidarians, platyhelminths, nemerteans, entoproctans, ectoproctans, annelids, hemichordates and urochordates are capable of somatic embryogenesis (Buss 1987;Blackstone & Jasker, 2003;Gustafson & Wessel, 2010;Rosner et al, 2009). Among arthropods, many parasitic rhizocephalan crustaceans (Rhizocephala: Cirripedia: Crustacea) have asexual reproduction, somatic embryogenesis by budding without separation of blastozooids resulting in the emergence of colonial organization (Høeg & Lützen, 1993, 1995Høeg et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Molecular and Sub-Cellular Gametogenic Machinery of Stem and Germline Cells Across Metazoa

Shukalyuk¹,

Isaeva²

2012

Current Frontiers and Perspectives in Cell Biology

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Phylogenetic considerations of clonality, coloniality, and mode of germline development in animals

Cited by 74 publications

References 41 publications

Early lineage specification of long-lived germline precursors in the colonial ascidianBotryllus schlosseri

Early lineage specification of long-lived germline precursors in the colonial ascidianBotryllus schlosseri

The Potential for Evolutionary Responses to Cell‐Lineage Selection on Growth Form and Its Plasticity in a Red Seaweed

Molecular and Sub-Cellular Gametogenic Machinery of Stem and Germline Cells Across Metazoa

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